Unusual Diversity of Apomictic Mechanisms in a Species of Miconia, Melastomataceae

Plant Systematics and Evolution (2018) 304:343–355 https://doi.org/10.1007/s00606-017-1480-1 ORIGINAL ARTICLE Unusual diversity of apomictic mechanisms in a species of Miconia, Melastomataceae Ana Paula S. Caetano1,2 · Priscila A. Cortez3 · Simone P. Teixeira4 · Paulo E. Oliveira5 · Sandra M. Carmello‑Guerreiro6 Received: 4 July 2017 / Accepted: 7 November 2017 / Published online: 5 December 2017 © Springer-Verlag GmbH Austria, part of Springer Nature 2017 Abstract Apomixis, the asexual formation of seeds, seems to be a reproductive alternative for many angiosperms, involving various pathways with diferent genetic and ecological consequences. It is common in some megadiverse tropical groups such as Melastomataceae, of which approximately 70% of the species studied so far in the tribe Miconieae are autonomous apom‑ ictics. Hence, Miconia appears to be a good model for the study of the embryological pathways associated with apomixis. In the present study, we analyzed the polyploid and autonomous apomictic M. fallax and compared its embryology to that of the diploid and sexual M. pepericarpa, both treelets species common in the Cerrado, the Neotropical savanna areas of Central Brazil. Ovule structure and basic megasporogenesis and megagametogenesis events were similar in both species. However, M. fallax showed exclusive features associated with apomixis: aposporous embryo sac development, with the par‑ thenogenetic development of unreduced egg cells, autonomous endosperm formation, nucellar embryony and polyembryony. Moreover, both gametophytic and sporophytic apomixis occurred in parallel to the development of a sexual embryo sac, a rarely described condition, which probably confers a great reproductive fexibility to the species. Keywords Adventitious embryony · Apospory · Autonomous apomixis · Megagametogenesis · Megasporogenesis · Polyembryony Introduction Handling editor: Hans de Jong. Despite the prevalence of sexual reproduction, apomixis— * Ana Paula S. Caetano the asexual production of seeds—is an alternative that seems [email protected] to have been important for the evolution and diversifcation of the angiosperms (Asker and Jerling 1992; Hojsgaard et al. 1 Programa de Pós‑Graduação em Ecologia e Conservação 2014). In general, the apomictic process bypasses important de Recursos Naturais, Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Minas Gerais, Brazil steps of sexual reproduction, notably both meiosis and egg cell fertilization, and has been viewed as a temporal and 2 Programa de Pós‑Graduação em Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, spatial deregulation of the sexual developmental program São Paulo, Brazil (Koltunow 1993; Koltunow and Grossniklaus 2003; Hand 3 Centro de Microscopia Eletrônica, Departamento de Ciências and Koltunow 2014). Currently, apomixis is considered an Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, important reproductive strategy often associated with geo‑ Bahia, Brazil graphical parthenogenesis and polyploidy (Carman 1997; 4 Departamento de Ciências Farmacêuticas, Faculdade de Hörandl et al. 2008; Santos et al. 2012). Ciências Farmacêuticas de Ribeirão Preto, Universidade de The seeds that result from the apomictic process can have São Paulo, Ribeirão Preto, São Paulo, Brazil embryos originating from a somatic cell of the ovule (sporo‑ 5 Instituto de Biologia, Universidade Federal de Uberlândia, phytic apomixis or adventitious embryony) or from an unfer‑ Uberlândia, Minas Gerais, Brazil tilized egg cell of an unreduced embryo sac (gametophytic 6 Departamento de Biologia Vegetal, Instituto de Biologia, apomixis). In the latter case, the unreduced embryo sac orig‑ Universidade Estadual de Campinas, Campinas, São Paulo, inates from a megaspore mother cell in which meiosis was Brazil Vol.:(0123456789)1 3 344 A. P. S. Caetano et al. suppressed or altered (diplospory), or from a nucellar cell species are concentrated mainly on herbaceous Asteraceae called aposporous initial (apospory), by mitotic divisions in from temperate regions (Koltunow et al. 1998, 2000; Van both cases (Asker and Jerling 1992; Crane 2001; Hand and Dijk 2003; Noyes 2007), members of the tropical and mostly Koltunow 2014). woody Miconieae represent alternative models for studies of More than one somatic cell in an ovule giving rise to autonomous apomixis. embryos is a common phenomenon in adventitious embry‑ Despite their pollinator independence, some apomic‑ ony (Naumova 1993; Batygina and Vinogradova 2007). tic Miconieae species may produce viable pollen (Caetano Moreover, the successful embryogenesis in an ovule with et al. 2013b; Maia et al. 2016). Because these species receive multiple embryo sacs, either aposporous embryo sacs or visits from pollinators (Maia et al. 2016), we hypothesized aposporous and sexual embryo sacs, can lead to polyem‑ that the sexual mechanism would co‑occur with the apom‑ bryony. Therefore, the sexual and asexual processes may ictic one. Secondly, we hypothesized that pollination‑inde‑ occur in the same or in diferent seeds in a given apomictic pendent species could produce an autonomous endosperm. species (Asker and Jerling 1992; Koltunow and Grossniklaus In this study, we show similar sexual events of megasporo‑ 2003; Batygina and Vinogradova 2007). Indeed, most plants genesis and megagametogenesis in the apomictic and polli‑ are facultative apomictic. From an evolutionary perspective, nation‑independent M. fallax DC. and its congener M. pep- the facultative apomixis seems to be advantageous by keep‑ ericarpa Mart. ex DC. Furthermore, M. fallax produces an ing both asexual and sexual reproductive modes (Koltunow autonomous endosperm, and the co‑occurrence of apospory, and Grossniklaus 2003; Hojsgaard and Hörandl 2015). On adventitious embryony and sexuality, leads to development the other hand, the apomixis is the only mode of reproduc‑ of polyembryonic seeds, showing a mixed reproductive strat‑ tion by seeds in obligate apomictic species (Koltunow 1993; egy in this markedly diverse group. Richards 1997), which have been pointed out as exceptions in natural populations (Nogler 1984; Asker and Jerling 1992; Hojsgaard and Hörandl 2015). Materials and methods Although apomixis usually bypasses sexual reproduction stages, not all apomicts are completely pollination independ‑ Plant materials ent. Most species are pseudogamous, which means that the nuclear fusion between the male gamete and the central cell The two species of Miconia studied here are common shrubs/ is required for functional endosperm development. Pseudog‑ trees in the Cerrado, the Neotropical savanna region of Cen‑ amous apomicts seem to be prevalent among species with tral Brazil, and have been previously studied for breeding adventitious embryony or apospory. Pseudogamy is unneces‑ system features by Goldenberg and Shepherd (1998). On sary only in autonomous apomicts, an apparently uncommon the one hand, the pollination‑independent, apomictic and condition, prevalent among diplosporous apomicts (Asker polyploid M. fallax is a shrub species with a wide distri‑ and Jerling 1992; Koltunow and Grossniklaus 2003; Whit‑ bution from Peru, Venezuela and Guiana to southeastern ton et al. 2008). Brazil. On the other hand, the diploid and sexual species M. Sporophytic and/or gametophytic apomixis has been pepericarpa is a Cerrado tree with a distribution restricted reported for 78 fowering plant families and has arisen sev‑ to some Brazilian states (Goldenberg and Shepherd 1998; eral times during the evolutionary history of angiosperms Goldenberg 2009; Caetano et al. 2013b). (Hojsgaard et al. 2014). Asteraceae, Poaceae and Rosaceae The samples were collected in Cerrado fragments of are historically cited as containing the majority of known Itirapina, São Paulo State, Brazil (lat. 22°15′10″S, long. apomictic genera (Carman 1997; Hojsgaard et al. 2014). 47°49′22″W). Voucher specimens were deposited in the However, the mostly tropical Melastomataceae has gained Herbarium of Universidade Estadual de Campinas (UEC), prominence due to their high frequency of autonomous São Paulo State, Brazil, under the numbers 150450 (M. fal- apomictic species, particularly within the tribe Miconieae, lax) and 150451 (M. pepericarpa). which contains up to 70% of apomictics species (Renner 1989; Goldenberg and Shepherd 1998; Goldenberg and Var‑ Megasporogenesis, megagametogenesis, assin 2001; Santos et al. 2012; Maia et al. 2016). and endosperm and apomictic embryo origin Studies concerning the cytological mechanisms of apomixis and their relation with sexuality within Mico‑ Megasporogenesis and megagametogenesis analyses for both nieae have revealed important insights that are useful for species were carried out using diferent developmental stages developmental, taxonomic and ecological knowledge, but from fower bud to fower anthesis. The origin of apomictic still involve a small percentage of species in this megad‑ embryos was determined also using seeds of M. fallax at iverse group (Borges 1991; Cortez et al. 2012; Caetano several developmental stages. Buds, fowers and fruits were et al. 2013a, b). Since studies with autonomous apomictic collected from six individuals per species. Finally, the origin 1 3 Sexual and apomictic development in Miconia, Melastomataceae 345 and development of autonomous endosperm in M. fallax was shared conditions, we observed some cytological difer‑ determined from three individuals using seeds obtained from ences, related to the reproductive

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